Identification and characterisation of β-carotene and retinol-producing commensal probiotic bacteria from liver, intestine and rumen tissues of grass-fed cattle
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Abstract
We hypothesised and investigated whether commensal probiotic bacteria from bovine organs are capable of synthesising β-carotene and retinol. A total of 111 potentially probiotic bacteria were isolated from the liver (β-carotene storage site), intestine (β-carotene bioconversion site) and rumen (β-carotene absorption site) tissues. Among these strains, 33 were screened based on vitamin A biosynthesis capability using UV spectroscopy and identified through matrix-assisted laser desorption/ionisation coupled with time-of-flight mass spectrometry analysis. Four Lactiplantibacillus plantarum (22.82 ± 1.85 to 111.95 ± 3.10 μg β-carotene gâ1 dry cell weight) and one Escherichia coli (44.77 ± 2.08 μg β-carotene gâ1 dry cell weight) strains with higher β-carotene and or retinol production capacity were further quantified through ultra (high) performance liquid chromatography-quadrupole-time of flight mass spectrometer. Lactiplantibacillus plantarum (VLL1) of liver origin showed good viability in gastric acid (pH 2.0) and bile salts (0.3%) and better tolerance in other probiotic properties. Hence, this study shows the β-carotene producing Lactiplantibacillus strains from the bovine origin as a potential source of vitamin A biofortification. Perhaps this study also establishes that the gut-friendly property of these probiotic strains with metabolic machinery for bioconversion of β-carotene to retinoids will be useful in eradicating vitamin A deficiency through probiotic therapy.
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Andrieux, C., Gadelle, D., Leprince, C. and Sacquet, E., 1989. Effects of some poorly digestible carbohydrates on bile acid bacterial transformations in the rat. British Journal of Nutrition 62: 103-119.
-
Aono, R. and Horikoshi, K., 1991. Carotenes produced by alkaliphilic yellow-pigmented strains of Bacillus. Agricultural and Biological Chemistry 55: 2643-2645.
-
Bhosale, P. and Bernstein, P.S., 2004. β-Carotene production by Flavobacterium multivorum in the presence of inorganic salts and urea. Journal of Industrial Microbiology & Biotechnology 31: 565-571.
-
Bindea, M., Rusu, B., Rusu, A., Trif, M., Leopold, L.F., Dulf, F. and Vodnar, D.C., 2018. Valorification of crude glycerol for pure fractions of docosahexaenoic acid and β-carotene production by using Schizochytrium limacinum and Blakeslea trispora. Microbial Cell Factories 17: 97.
-
Charteris, W.P., Kelly, P.M., Morelli, L. and Collins, J.K., 1998. Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. Journal of Applied Microbiology 84: 759-768.
-
Cherkaoui, A., Hibbs, J., Emonet, S., Tangomo, M., Girard, M., Francois, P. and Schrenzel, J., 2010. Comparison of two matrix-assisted laser desorption ionization-time of flight mass spectrometry methods with conventional phenotypic identification for routine identification of bacteria to the species level. Journal of Clinical Microbiology 48: 1169-1175.
-
Conboy Stephenson, R., Ross, R.P. and Stanton, C., 2021. Carotenoids in milk and the potential for dairy based functional foods. Foods 10.
-
During, A., Nagao, A., Hoshino, C. and Terao, J., 1996. Assay of β-carotene 15, 15â²-dioxygenase activity by reverse-phase high-pressure liquid chromatography. Analytical Biochemistry 241: 199-205.
-
Elegbeleye, J.A., Krishnamoorthy, S., Bamidele, O.P., Adeyanju, A.A., Adebowale, O.J. and Agbemavor, W.S.K., 2022. Health-promoting foods and food crops of West-Africa origin: the bioactive compounds and immunomodulating potential. Journal of Food Biochemistry 46: e14331.
-
GarcıÌa-LoÌpez, E., GonzaÌlez-Gallardo, A., AntaramiaÌn, A., GonzaÌlez-DaÌvalos, M.L., Shimada, A., Varela-Echavarria, A. and Mora, O., 2012. In vitro conversion of Ã-carotene to retinal in bovine rumen fluid by a recombinant Ã-carotene-15, 15â²-monooxygenase. International Journal for Vitamin and Nutrition Research 82: 94-103.
-
Garrido-FernaÌndez, J., Juan Maldonado-BarragaÌn, A., Caballero-Guerrero, B., Hornero-MeÌndez, D. and Ruiz-Barba, J.L., 2010. Carotenoid production in Lactobacillus plantarum. International Journal of Food Microbiology 140: 34-39.
-
Green, A.S. and Fascetti, A.J., 2016. Meeting the vitamin a requirement: the efficacy and importance of β-carotene in animal species. The Scientific World Journal 2016: 22.
-
Hinchliffe, E., Rudge, J. and Reed, P., 2015. A novel high-throughput method for supported liquid extraction of retinol and alpha-tocopherol from human serum and simultaneous quantitation by liquid chromatography tandem mass spectrometry. Annals of Clinical Biochemistry 53: 434-445.
-
Iyer, N. and Vaishnava, S., 2019. Vitamin A at the interface of host-commensal-pathogen interactions. PLoS Pathogens 15: e1007750.
-
Jaglan, N., Kumar, S., Choudhury, P.K., Tyagi, B. and Tyagi, A.K., 2019. Isolation, characterization and conjugated linoleic acid production potential of bifidobacterial isolates from ruminal fluid samples of Murrah buffaloes. Anaerobe 56: 40-45.
-
Jang, H.J., Yoon, S.H., Ryu, H.K., Kim, J.H., Wang, C.L., Kim, J.Y., Oh, D.K. and Kim, S.W., 2011. Retinoid production using metabolically engineered Escherichia coli with a two-phase culture system. Microbial Cell Factories 10: 59.
-
Jose, N., Bunt, C. and Hussain, M., 2015. Comparison of microbiological and probiotic characteristics of lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms 3: 198-212.
-
Keating, N. and Keely, S.J., 2009. Bile acids in regulation of intestinal physiology. Current Gastroenterology Reports 11: 375-382.
-
Kim, M., Jung, D.-H., Seo, D.-H., Park, Y.-S. and Seo, M.-J., 2021. 4, 4â²-diaponeurosporene from Lactobacillus plantarum subsp. plantarum KCCP11226: low temperature stress-induced production enhancement and in vitro antioxidant activity. Journal of Microbiology and Biotechnology 31: 63-69.
-
Kleerebezem, M., Boekhorst, J., Van Kranenburg, R., Molenaar, D., Kuipers, O.P., Leer, R., Tarchini, R., Peters, S.A., Sandbrink, H.M., Fiers, M.W., Stiekema, W., Lankhorst, R.M., Bron, P.A., Hoffer, S.M., Groot, M.N., Kerkhoven, R., de Vries, M., Ursing, B., de Vos, W.M. and Siezen, R.J., 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proceedings of the National Academy of Sciences of the United States of America 100: 1990-1995.
-
Krishnamoorthy, S., Arunkumar, A., Baskaran, N., Rawson, A. and Vignesh, S., 2023. Food microbiome. 1st ed. Gothandam, K.M., Srinivasan, R., Ranjan, S. and Dasgupta, N. (eds.). CRC Press.
-
Krishnamoorthy, S. and Buys, E.M., 2019. Insights into the role of bacteria in vitamin A biosynthesis: future research opportunities. Critical Reviews in Food Science and Nutrition 59: 3211-3226.
-
Kumaravel, S. and Srinivasan, K., 2017. Antioxidant and antimicrobial activity of silver nanoparticles synthesized using Cinnamomum zeylanicum: 8-12.
-
Li, P., Gu, Q., Yang, L., Yu, Y. and Wang, Y., 2017. Characterization of extracellular vitamin B12 producing Lactobacillus plantarum strains and assessment of the probiotic potentials. Food Chemistry 29: 105-109.
-
Masuda, M., Ide, M., Utsumi, H., Niiro, T., Shimamura, Y. and Murata, M., 2012. Production potency of folate, vitamin B12, and thiamine by lactic acid bacteria isolated from Japanese pickles. Bioscience, Biotechnology, and Biochemistry 76: 2061-2067.
-
Miller, J.K., Harrison, M.T., DâAndrea, A., Endsley, A.N., Yin, F., Kodukula, K. and Watson, D.S., 2013. β-Carotene biosynthesis in probiotic bacteria. Probiotics and Antimicrobial Proteins 5: 69-80.
-
Mohd Adnan, A.F. and Tan, I.K.P., 2007. Isolation of lactic acid bacteria from Malaysian foods and assessment of the isolates for industrial potential. Bioresource Technology 98: 1380-1385.
-
OâSullivan, E. and Condon, S., 1997. Intracellular pH is a major factor in the induction of tolerance to acid and other stresses in Lactococcus lactis. Applied and Environmental Microbiology 63: 4210-4215.
-
Plozza, T., Craige Trenerry, V. and Caridi, D., 2012. The simultaneous determination of vitamins A, E and β-carotene in bovine milk by high performance liquid chromatography-ion trap mass spectrometry (HPLC-MS n). Food Chemistry 134: 559-563.
-
Rasika, D.M.D., Vidanarachchi, J.K., Luiz, S.F., Azeredo, D.R.P., Cruz, A.G. and Ranadheera, C.S., 2021. Probiotic delivery through non-dairy plant-based food matrices. Agriculture 11.
-
Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I. and Tuohy, K., 2018. Gut microbiota functions: metabolism of nutrients and other food components. European Journal of Nutrition.
-
Silva, C., Cabral, J.M.S. and van Keulen, F., 2004. Isolation of a β-carotene over-producing soil bacterium, Sphingomonas sp. Biotechnology Letters 26: 257-262.
-
Takemura, M., Takagi, C., Aikawa, M., Araki, K., Choi, S.-K., Itaya, M., Shindo, K. and Misawa, N., 2021. Heterologous production of novel and rare C(30)-carotenoids using Planococcus carotenoid biosynthesis genes. Microbial Cell Factories 20: 194.
-
Tang, G., Hu, Y., Yin, S., Wang, Y., Dallal, G.E., Grusak, M.A. and Russell, R.M., 2012. β-Carotene in golden rice is as good as β-carotene in oil at providing vitamin A to children. The American Journal of Clinical Nutrition 96: 658-664.
-
UNICEF, 2023. Nearly two in three children in need were protected with the requisite two annual high dose vitamin A supplements in 2022.
-
Veloo, A.C.M., Welling, G.W. and Degener, J.E., 2011. The identification of anaerobic bacteria using MALDI-TOF MS. Anaerobe 17: 211-212.
-
Welker, M. and Moore, E.R.B., 2011. Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Systematic and Applied Microbiology 34: 2-11.
-
Wyss, A., Wirtz, G.M., Woggon, W.D., Brugger, R., Wyss, M., Friedlein, A., Riss, G., Bachmann, H. and Hunziker, W., 2001. Expression pattern and localization of β, β-carotene 15, 15â²-dioxygenase in different tissues. Biochemical Journal 354: 521-529.
-
Yoon, S.H., Park, H.M., Kim, J.E., Lee, S.H., Choi, M.S., Kim, J.Y., Oh, D.K., Keasling, J.D. and Kim, S.W., 2007. Increased β-carotene production in recombinant Escherichia coli harboring an engineered isoprenoid precursor pathway with mevalonate addition. Biotechnology Progress 23: 599-605.
Supplementary Materials
| All Time | Past 365 days | Past 30 Days | |
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| Abstract Views | 292 | 292 | 29 |
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Identification and characterisation of β-carotene and retinol-producing commensal probiotic bacteria from liver, intestine and rumen tissues of grass-fed cattle
In: Beneficial MicrobesSearch for other papers by S. Krishnamoorthy in
Current site
Google Scholar
PubMed
Search for other papers by E.M. Buys in
Current site
Google Scholar
PubMed
Abstract
We hypothesised and investigated whether commensal probiotic bacteria from bovine organs are capable of synthesising β-carotene and retinol. A total of 111 potentially probiotic bacteria were isolated from the liver (β-carotene storage site), intestine (β-carotene bioconversion site) and rumen (β-carotene absorption site) tissues. Among these strains, 33 were screened based on vitamin A biosynthesis capability using UV spectroscopy and identified through matrix-assisted laser desorption/ionisation coupled with time-of-flight mass spectrometry analysis. Four Lactiplantibacillus plantarum (22.82 ± 1.85 to 111.95 ± 3.10 μg β-carotene gâ1 dry cell weight) and one Escherichia coli (44.77 ± 2.08 μg β-carotene gâ1 dry cell weight) strains with higher β-carotene and or retinol production capacity were further quantified through ultra (high) performance liquid chromatography-quadrupole-time of flight mass spectrometer. Lactiplantibacillus plantarum (VLL1) of liver origin showed good viability in gastric acid (pH 2.0) and bile salts (0.3%) and better tolerance in other probiotic properties. Hence, this study shows the β-carotene producing Lactiplantibacillus strains from the bovine origin as a potential source of vitamin A biofortification. Perhaps this study also establishes that the gut-friendly property of these probiotic strains with metabolic machinery for bioconversion of β-carotene to retinoids will be useful in eradicating vitamin A deficiency through probiotic therapy.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 292 | 292 | 29 |
| Full Text Views | 9 | 9 | 1 |
| PDF Views & Downloads | 26 | 26 | 3 |
